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A High-Resolution Anatomical Ontology of the Developing Murine Genitourinary Tract

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A High-Resolution Anatomical Ontology of the Developing Murine Genitourinary Tract Gene Expression Patterns 7 (2007) 680–699 www.elsevier.com/locate/modgep A high-resolution anatomical ontology of the developing murine genitourinary tract Melissa H. Little a,*,1, Jane Brennan b,1, Kylie Georgas a,1, Jamie A. Davies b,1, Duncan R. Davidson c,1, Richard A. Baldock c, Annemiek Beverdam a, John F. Bertram d, Blanche Capel e, Han Sheng Chiu a, Dave Clements c, Luise Cullen-McEwen d, Jean Fleming f, Thierry Gilbert a,2, Doris Herzlinger l, Derek Houghton c, Matt H. Kaufman b, Elena Kleymenova h, Peter A. Koopman a, Alfor G. Lewis i, Andrew P. McMahon j, Cathy L. Mendelsohn g, Eleanor K. Mitchell d, Bree A. Rumballe a, Derina E. Sweeney b, M. Todd Valerius j, Gen Yamada k, Yiya Yang c, Jing Yu j a Institute for Molecular Bioscience, University of Queensland, Brisbane 4072, Australia b Centre for Integrative Physiology, Edinburgh University, Edinburgh, UK c MRC Human Genetics Unit, Western General Hospital, Edinburgh, UK d Department of Anatomy and Cell Biology, Monash University, Melbourne, Australia e Department of Cell Biology, Duke University Medical Centre, Durham, NC, USA f Eskitis Institute of Cell and Molecular Therapies, Griffith University, Brisbane, Australia g Department of Urology and Pathology, Columbia University, NY, USA h CIIT Centers for Health Research, Research Triangle Park, NC 27709, USA i Division of Pediatric Urology, Cincinnati Children’s Hospital Research Foundation, Cincinnati, USA j Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA k Centre for Animal Resources and Development (CARD), Kumamoto University Honjo, Kumamoto, Japan l Cornell University Graduate School of Medical Sciences, Physiology and Biophysics, New York, NY 10021, USA Received 12 January 2007; received in revised form 14 March 2007; accepted 14 March 2007 Available online 23 March 2007 Abstract Cataloguing gene expression during development of the genitourinary tract will increase our understanding not only of this process but also of congenital defects and disease affecting this organ system. We have developed a high-resolution ontology with which to describe the subcompartments of the developing murine genitourinary tract. This ontology incorporates what can be defined histolog- ically and begins to encompass other structures and cell types already identified at the molecular level. The ontology is being used to annotate in situ hybridisation data generated as part of the Genitourinary Development Molecular Anatomy Project (GUDMAP), a publicly available data resource on gene and protein expression during genitourinary development. The GUDMAP ontology encom- passes Theiler stage (TS) 17–27 of development as well as the sexually mature adult. It has been written as a partonomic, text-based, hierarchical ontology that, for the embryological stages, has been developed as a high-resolution expansion of the existing Edinburgh Mouse Atlas Project (EMAP) ontology. It also includes group terms for well-characterised structural and/or functional units comprising several sub-structures, such as the nephron and juxtaglomerular complex. Each term has been assigned a unique identification number. Synonyms have been used to improve the success of query searching and maintain wherever possible existing EMAP terms relating to this organ system. We describe here the principles and structure of the ontology and provide representative diagrammatic, histological, * Corresponding author. Tel.: +61 7 3346 2054; fax: +61 7 33462101. E-mail address: [email protected] (M.H. Little). 1 major contributors. 2 INSERM, Paris. 1567-133X/$ - see front matter Ó 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.modgep.2007.03.002 M.H. Little et al. / Gene Expression Patterns 7 (2007) 680–699 681 and whole mount and section RNA in situ hybridisation images to clarify the terms used within the ontology. Visual examples of how terms appear in different specimen types are also provided. Ó 2007 Elsevier B.V. All rights reserved. Keywords: Genitourinary development; Renal development; Kidney development; Urinary development; Reproductive development; Kidney; Gonad; Bladder; Ureter; Urethra; Genital tubercle; Ovary; Testis; Congenital defects; Gene expression; Ontology; Annotation; Database; Anatomy; Atlas of development; Partonomic ontology; RNA in situ hybridisation 1. Results and discussion Postnatal-onset disease of the urogenital tract is also a major problem. Cancer can arise in all parts of the urogen- 1.1. Development and disorders of the genitourinary tract ital tract with prostatic cancer showing the highest preva- lence (http://info.cancerresearchuk.org/cancerstats/incidence/ The vertebrate genitourinary tract comprises the urinary prevalence/). Some cancers of the urogenital tract (gonado- system (kidneys, ureters, bladder, urethra) and the repro- blastoma, Wilms’ tumour) represent a persistence of the ductive system (external genitalia, prostate, gonads, associ- embryonic state. Chronic renal disease, due to polycystic ated ducts (fallopian tubes, vas deferens and epididymis) kidney disease, cardiovascular disease, injury, infection, and uterus). The genitourinary tract arises from both meso- glomerulonephritis or diabetes, results in end stage renal dermal and endodermal components, but the intersection disease (ESRD). The link between development and renal of these components occurs early in development and ulti- disease comes from evidence that the number of nephrons mately they are so closely linked that congenital anomalies present in each kidney is inversely correlated with the or damage in one part frequently affects the other. The kid- chance of chronic renal disease later in life (Hoy et al., neys, ureters and internal genitalia (gonads, uterus, ovi- 2005). Conversely, adult onset renal disease and other dis- ducts, epididymis and vas deferens) arise from the orders of the genitourinary tract show reactivation of mol- intermediate mesoderm. The urethra and bladder form ini- ecules key to the normal development of the genitourinary tially as part of the endodermal cloaca. The urorectal sep- tract. tum divides the cloaca to form the urogenital sinus on the ventral side and the hindgut on the dorsal side. The exter- 1.2. The Genitourinary Development Murine Atlas Project nal genitalia form from the genital tubercle that, like the gonads, is initially undifferentiated. At eight weeks of All these observations highlight the need to comprehen- human gestation, sex determination occurs and, four weeks sively understand the molecular basis of genitourinary later, hormones produced from the gonads direct the devel- development. While this understanding is not attainable opment either of clitoris and labia or penis and scrotum. in humans, the need has catalysed the creation of the Gen- The European Surveillance of Congenital Anomalies, itourinary Development Molecular Anatomy Project Eurocat, reported that in Europe between 1996 and 2001, (GUDMAP). GUDMAP aims to chronicle the expression congenital anomalies of the internal genitourinary tract of genes, both temporally and spatially, during the devel- (excluding external genitalia) represented the third most opment and maturation of the murine genitourinary tract frequent of all human birth defects, occurring in approxi- and to create tools for the scientific community to examine mately 28/10,000 live births (Eurocat Annual Report, the biological function of these genes. The creation of an 2003). Only cardiovascular (61/10,000) and limb atlas of gene expression will serve as a reference point in (37/10,000) defects were more prevalent. Genitourinary analyses of lineage, cell fate and disease within this organ defects can vary from severe (bladder exstrophy, posterior system. Gene expression data to be held in the atlas will urethral valves, persistent cloaca, cystic kidney disease, include microarray, RNA in situ hybridisation and immu- hydronephrosis, streak gonads, diphallia) to more moder- nohistochemical information. Well-characterized markers ate (hypospadias, horseshoe kidney, micropenis, cryptor- of structures within the genitourinary tract will also help chidism, unilateral renal agenesis). Some of these defects to standardize mutant analyses and enable more subtle (e.g.horseshoe kidney, unilateral renal agenesis) do not phenotypes to be recognised. Data generated within this require surgical intervention and may not even be diag- project are being made freely publicly available via a cen- nosed (Weizer et al., 2002), while others may require exten- tral database (http://www.gudmap.org). The need for these sive reconstructive surgery. The latter include bladder data to be annotated accurately was a driving force in the reconstruction for persistent cloaca, organ transplantation development of a text-based anatomical ontology of the for cystic kidney disease and renal dysgenesis, removal of genitourinary tract. By developing a defined ontology, this streak gonads and Mu¨llerian duct remnants for XY pseu- will enable the efficient computational linking of different dohermaphroditism and penile reconstruction for hypospa- types of molecular analyses (e.g. microarray and in situ dias and diphallia (Gyftopoulos et al., 2002; Warne et al., hybridisation) adding to our understanding of develop- 2002). The developmental relationship between the urinary ment at a systems biology level. and reproductive systems is strongly reflected in the combi- The Edinburgh Mouse Atlas Project (EMAP; http:// nation of observed defects. genex.hgu.mrc.ac.uk/intro.html)
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